Vol. 6: 113–125, 2008 ENDANGERED SPECIES RESEARCH Printed December 2008 doi: 10.3354/esr00087 Endang Species Res Published online May 7, 2008

Contribution to the Theme Section ‘The IUCN Red List of Threatened Species: assessing its utility and value’ OPENPEN ACCESSCCESS REVIEW Conservation planning and the IUCN Red List

M. Hoffmann1, 2,*, T. M. Brooks1, 3, 4, G. A. B. da Fonseca5, 6, C. Gascon 7, A. F. A. Hawkins7, R. E. James8, P. Langhammer9, R. A. Mittermeier7, J. D. Pilgrim10, A. S. L. Rodrigues11, J. M. C. Silva12

1Center for Applied Biodiversity Science, Conservation International, 2011 Crystal Drive Suite 500, Arlington, Virginia 22202, USA 2IUCN Species Programme, IUCN — International Union for the Conservation of Nature, Rue Mauverney, 1196 Gland, Switzerland 3World Agroforestry Center (ICRAF), University of the Philippines Los Baños, Laguna 4031, Philippines 4School of Geography and Environmental Studies, University of Tasmania, Hobart, Tasmania 7001, Australia 5Global Environment Facility, 1818 H Street NW, Washington, DC 20433, USA 6Departamento de Zoologia, Universidade Federal de Minas Gerais, Avenida Antonio Carlos 6627, Belo Horizonte MG 31270-901, Brazil 7Conservation International, 2011 Crystal Drive Suite 500, Arlington, Virginia 22202, USA 8Conservation International Melanesia Centre for Biodiversity Conservation, PO Box 106, Waigani, NCD, Papua New Guinea 9School of Life Sciences, Arizona State University, PO Box 874501, Tempe, Arizona 85287-4501, USA 10BirdLife International in Indochina, N6/2+3, Ngo 25, Lang Ha, Ba Dinh, Hanoi, Vietnam 11Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, UK 12Conservation International — Brazil, Av. Gov. José Malcher 652, 2o. Andar, Ed. CAPEMI, Bairro: Nazaré, 66035-100, Belém, Pará, Brazil

ABSTRACT: Systematic conservation planning aims to identify comprehensive protected area net- works that together will minimize biodiversity loss. Importantly, conservation planners seek to deter- mine where to allocate limited resources first, particularly given the uneven spread of, and threats to, biodiversity. The International Union for the Conservation of Nature (IUCN) Red List of Threatened Species incorporates data not only on threats to species, but also on species distributions and ecolog- ical requirements. These temporal and spatial attributes, when combined with other datasets, have proven useful for determining the most urgent priority areas for conserving biodiversity, from the global level down to the scale of individual sites. Although many challenges remain, the increasing reliability and comprehensiveness of the IUCN Red List suggests that its role as a source of biodiver- sity data in systematic conservation planning is certain to expand dramatically.

KEY WORDS: IUCN Red List · Conservation planning · Threatened species · Biodiversity conservation · Protected areas

Resale or republication not permitted without written consent of the publisher

INTRODUCTION to guide conservation responses, primarily by identify- ing key and priority habitats for species, sites to be The International Union for the Conservation of safeguarded, and actions required (Collar 1993–4, Nature (IUCN) Red List of Threatened Species (www. 1996a). While current IUCN guidelines (Standards and iucnredlist.org; hereafter referred to as the IUCN Red Petitions Working Group 2006) are explicit that the List) is the accepted standard for species global extinc- IUCN Red List should not be used in isolation for set- tion risk (Lamoreux et al. 2003, Rodrigues et al. 2006). ting priorities or determining conservation responses, Traditionally, the IUCN Red List has served not only to the IUCN Red List and conservation priority setting highlight species at greatest risk of extinction, but also have proven inseparable (Mace & Lande 1991, Mace

*Email: [email protected] © Inter-Research 2008 · www.int-res.com 114 Endang Species Res: 6:113–125, 2008

1995). Both governmental and non-governmental rigues et al. 2006). An initial driving force behind this organizations increasingly rely on the IUCN Red List to transformation was the role of such lists in setting pri- inform priorities, influence legislation, and guide con- orities for conservation, especially at the level of pri- servation investment, particularly as its influence con- oritizing among species. The qualitatively defined tinues to grow (Fig. 1). One recent case concerns the categories and definitions were criticized for being new Resource Allocation Framework of the Global subjective, raising concerns that assessments made Environment Facility (GEF; the financial mechanism of by different authorities did not accurately reflect true the Convention on Biological Diversity) that incorpo- extinction risks and skewed conservation priorities rates IUCN Red List data to provide a relative ranking (Master 1991). of countries for meeting the biodiversity objectives A revised risk-ranking system, incorporating quanti- of the GEF (www.gefweb.org/documents/council_ tative categories and criteria (Mace & Lande 1991), documents/GEF_C27/documents/C.27.Inf.8.Rev.1_RAF. and adopted in 1994 (IUCN 1994), presented several pdf). Although this profile has resulted in some degree advances, notably (1) enabling consistent application of misuse, especially in the wake of a paucity of guid- by different people, (2) being based around probabilis- ance on its appropriate application, it nevertheless tic assessment of extinction risk, (3) incorporation of a provides a particularly important example of the time-scale; (4) flexibility of data required and popula- power of the IUCN Red List to inform policy. Here, we tion units to which it applied, and (5) ability to handle briefly review the development of the IUCN Red List uncertainty (Mace & Lande 1991). Whereas the first and its function in conservation planning, specifically, IUCN Red List assessments depended on knowledge in identifying priority areas for biodiversity conserva- complemented by a large dose of subjective common tion; we also discuss challenges to improving its utility sense, these new categories and criteria were designed for this purpose. This review is particularly timely, to improve repeatability and consistency in the listing because IUCN members have passed a resolution that process. identifies conservation planning as one of the most Since the adoption of the most recent revision to the important areas for future expansion (Resolution criteria in 2001 (IUCN 2001; Fig. 2, Table 1), there has RESWCC3.013 of the 2004 World Conservation Con- been considerable emphasis on improving the taxo- gress). nomic coverage, rigor, justification, and transparency of IUCN Red List assessments. For example, partly in response to criticisms (e.g. Mrosovsky 1997), assess- EVOLUTION OF THE IUCN RED LIST ments are now underpinned by mandatory supporting documentation, including information on geographic Red Data Books were first conceived in the early range and abundance, habitats, threats, and conserva- 1960s, as a ‘register of threatened wildlife that tion actions (see www.iucnredlist.org); these assess- includes definitions of degrees of threat’ (Fitter & Fit- ments are consultative, now increasingly facilitated ter 1987). Since then they have undergone significant through workshops and web-based open-access sys- evolution from simple lists of species and categories tems (e.g. BirdLife International’s Globally Threatened into an increasingly comprehensive compendium of Bird forums; www.birdlifeforums.org), and peer-re- conservation-related information on species (Rod- viewed. As such, today’s IUCN Red List is promoted not only as a credible and objective source of species’ 300 threat status with a remit beyond the cause of a few 250 handpicked species, but as a growing data mine, which has improved its utility in conservation, includ- 200 ing species-based conservation, policy and manage- 150 ment, biodiversity evaluation, and monitoring (Rod- rigues et al. 2006). 100 No. of citations 50 EVOLUTION OF CONSERVATION PLANNING 0 1989 1991 1993 1995 1997 1999 2001 2003 Year Priority-setting approaches that identify global prior- Fig. 1. Number of citations of the IUCN Red List per year, in ities for conservation, such as the Global 200 eco- peer-reviewed journals, up to and including 2004. Total of regions (Olson & Dinerstein 1998), biodiversity 1047 citations (Web of Science, http://isiwebofknowledge. com, April 25, 2005), either on the topic ‘Red List’ + ‘IUCN’, or hotspots (Myers et al. 2000), and Endemic Bird Areas citing at least one of the IUCN Red List main publications, (Stattersfield et al. 1998), have proven effective at or both directing conservation resources at a global scale to Hoffmann et al.: Conservation planning and the IUCN Red List 115

Fig. 2. The IUCN Red List categories (adapted, with permission, from IUCN 2001) those regions most urgently in need of conservation 90% of threatened mammals, birds and amphibians; investment (Brooks et al. 2006). However, these Baillie et al. 2004). Consequently, area-based action, or approaches are not designed, nor intended, to inform more specifically the mitigation of threats by means of the identification of more fine-scale targets for conser- the establishment of protected areas, is the most effec- vation action, such as actual sites with biodiversity fea- tive conservation response for safeguarding biodiver- tures that require safeguarding. sity (Bruner et al. 2001, Oliveira et al. 2007) — albeit not For most biodiversity, habitat loss and degradation is necessarily sufficient to ensure long-term viability in the most pervasive threat (affecting, for example, 85 to the face of threats such as climate change (Pounds et al.

Table 1. Simplified overview of the IUCN Red List criteria (adapted, with permission, from Butchart et al. 2004) (see IUCN 2001, Standard and Petitions Working Group 2006). EOO: extent of occurrence; AOO: area of occupancy; na: not applicable

Criterion Critically Endangered Vulnerable Qualifiers and notes Endangered (EN) (VU) (CR)

A1: reduction in population size ≥90% ≥70% ≥50% Over 10 yr/3 generationsa in the past, where causes of the reduction are clearly reversible AND understood AND have ceased A2–4: reduction in population size ≥80% ≥50% ≥30% Over 10 yr/3 generationsa in past, future or combination B1: small range (EOO) <100 km2 <5000 km2 <20 000 km2 Plus 2 of (1) severe fragmentation/few locations (1, ≤5, ≤10), (2) continuing decline, (3) extreme fluctuation B2: small range (AOO) <10 km2 <500 km2 <2000 km2 Plus 2 of (1) severe fragmentation/few locations (1, ≤5, ≤10), (2) continuing decline, (3) extreme fluctuation C: small and declining population <250 <2500 <10 000 Mature individuals. Continuing decline either (1) over specified rates and time periods or (2) with (a) specified popula- tion structure or (b) extreme fluctuation D1: very small population <50 <250 <1000 Mature individuals D2: very restricted population na na <20 km2 AOO or Capable of becoming Critically Endan- ≤5 locations gered or even Extinct within a very short time frame E: quantitative analysis ≥50% in ≥20% in ≥10% in Estimated extinction-risk using quanti- 10 yr/ 10 yr/ 100 yr tative models (e.g. population viability 3 generationsa 5 generationsa analysis aWhichever is longer 116 Endang Species Res: 6:113–125, 2008

2006) or disease (Walsh et al. 2003). Since forest rem- be opportunity-driven, as there are plenty of spatial nants in fragmented landscapes that are already pro- options. This may translate in conserving first the sites tected or available for conservation are often at high of lower vulnerability, as they are often those where risk of loss (Gascon et al. 2000), conservation planning conservation costs are lower and thus opportunity also considers matrix-level interventions that would im- higher. Conceptually, all of the 9 global biodiversity prove the likelihood of the permanence of current inter- conservation priority setting schemes fit within this ventions (e.g. da Fonseca et al. 2005). Such interven- framework of irreplaceability relative to vulnerability tions represent a biodiversity conservation strategy in (Brooks et al. 2006). their own right (Szaro & Johnston 1996, Boyd et al. in In the long term, persistence of species requires not press), but are not the focus of the present paper. only maximizing their representation in places where Conservation planning aims to optimize the alloca- they are currently present, but crucially also minimiz- tion of limited conservation resources by identifying ing the probability of their being lost (Pressey et al. comprehensive networks of sites or protected areas 2004). Scheduling priorities for conservation according that together will contribute to the overall goal of min- to combined irreplaceability and vulnerability in- imizing biodiversity loss (Pressey et al. 1993, Margules creases retention, as it focuses efforts on the places & Pressey 2000). This is particularly necessary since more likely to lose unique biodiversity (Pressey et al. threats to biodiversity are distributed unevenly, with 2004). Furthermore, ensuring species persistence also the result that investments must be made in some requires the conservation of the ecological processes places with greater urgency than others, in order to on which they rely (Pressey et al. 2003). This is partic- prevent the loss of unique biodiversity. The significant ularly important at the finer scales at which individual advances made in the field of systematic conservation protected areas are created. planning over the past 2 decades (e.g. Kirkpatrick 1983, Margules & Pressey 2000), have seen the science move beyond theory to actual on-the-ground applica- USE OF THE IUCN RED LIST tion (e.g. Cowling et al. 2003). Such strategic decision-making requires information Informing spatial options on both the spatial and temporal options available for in- clusion in the planning framework. These 2 variables are Information on the distribution and ecological commonly referred to as irreplaceability and vulnerabil- requirements of species can help determine spatial ity, respectively, in the conservation planning literature options for biodiversity conservation. The most signifi- (Pressey & Taffs 2001). Irreplaceability is a measure of cant recent innovation of the IUCN Red List is the the degree to which the spatial options available for con- incorporation of spatial data. Range maps representing servation of unique biodiversity features are lost if that extent of occurrence (EOO1) are now available for particular site is lost. At its most extreme, for example, a nearly all the world’s mammals, birds, and amphibians site containing the entire population of a species (e.g. (Brooks et al. 2004). EOO data have proved extremely Ricketts et al. 2005) is wholly irreplaceable — there are valuable in large-scale analyses, such as identifying no other sites available (i.e. spatial options) for the con- centers of endemism (e.g. Orme et al. 2005), and servation of that species (Pressey et al. 1994). assessing the comprehensiveness of existing protected Vulnerability can be seen as a measure of irreplace- area networks and identifying gaps in coverage (e.g. ability, but on a temporal (i.e. time-sensitive) scale. Rodrigues et al. 2004b). Rondinini et al. (2005) used Just as threatened species are more likely to be lost information on habitat preferences to build habitat before non-threatened species, our options for con- suitability models within geographic range (EOO) data serving those sites facing high levels of vulnerability or to derive an estimated area of occupancy for African threat are more limited in time, with places of higher vertebrates in order to better assess shortfalls in the threat likely to lose their biodiversity value sooner continent’s reserve network. EOO data also inform (Rodrigues et al. 2004a). Vulnerability combines with conservation planning for area-demanding species, irreplaceability in complex ways to help define conser- such as vultures, that require coordinated conservation vation priorities. Sites of simultaneously high values action at regional or even continental scales (BirdLife for both variables are the obvious highest priorities as International 2004b, Boyd et al. in press). they correspond to places where the loss of unique bio- diversity is most imminent. Sites of high irreplaceabil- 1 ity and low vulnerability require conservation but can Defined by IUCN (2001) as ‘the area contained within the shortest continuous imaginary boundary which can be afford to wait, often providing great opportunities for drawn to encompass all the known, inferred or projected proactive, well-planned, conservation planning. Con- sites of present occurrence of a taxon, excluding cases of servation in low irreplaceability regions can afford to vagrancy’ Hoffmann et al.: Conservation planning and the IUCN Red List 117

However, EOO data have a coarse resolution and Red List data provide valuable information for the generally are useful only for highlighting priorities at identification of the processes (Pressey et al. 2003) that very large global or continental scales. To inform deci- must be considered to ensure species’ long-term per- sion-making at the site level, the level at which conser- sistence (e.g. interactions with other species, changes vation implementation actually takes place, much finer in fire regime, disruption of migratory routes). spatial data are required (e.g. Pressey et al. 2003). For Threatened species data have been used to highlight example, the identification of Important Bird Areas places where threatened biodiversity lacks protection (IBAs), developed and promoted by BirdLife Interna- and is, therefore, likely to be lost sooner, from the tional since the early 1980s (Osieck & Mörzer Bruyns national (e.g. Komar 2002, Danielsen & Treadaway 1981), has been facilitated by the compilation of local- 2004) to the global level. For example, Rodrigues et al. ity data for threatened species in Red Data Books, (2004a) highlighted priority regions for expanding the which subsequently enables ‘site-specific synthesis’ global protected-area network by incorporating a mea- (Collar 1993–4). Thus, initial identification of ‘Key sure, weighted by extinction risk, of the number of spe- forests for threatened birds in Africa’ (Collar & Stuart cies in each IUCN Red List category (Fig. 3). 1988) and ultimately of ‘Important Bird Areas in Africa Presence of threatened species also represents the and Associated Islands’ (Fishpool & Evans 2001) grew 4th (and primary) criterion for designating IBAs. Of the directly from the publication of ‘Threatened birds of 7504 IBAs of global significance identified in 188 coun- Africa and related islands’ (Collar & Stuart 1985). tries to date (Fig. 4; updated from BirdLife International Three of the 4 quantitative criteria used to identify 2004a). 66% were triggered based on the presence of a IBAs are intended to account for irreplaceability, by globally threatened species (M. Crosby pers. comm.). identifying sites2 holding significant populations of Increasingly, the IBA approach is being extended to species that are restricted in range, congregatory, or other taxa, and has led to the identification of, among characteristic (as an assemblage) of a biome (Fishpool others, Important Plant Areas (Anderson 2002) and im- & Evans 2001). portant sites for freshwater biodiversity (Darwall & Vié 2005). To create a unified set of criteria and a taxon- neutral umbrella for these initiatives, Eken et al. (2004) Informing temporal options introduced the concept of Key Biodiversity Areas (KBAs) an approach that builds on the strengths and Information on threats and on the vulnerability of underlying methodology of IBAs. Currently, KBAs for areas and species to these threats helps inform tempo- non-avian taxa have been identified and are being ral options for biodiversity conservation, improving safeguarded in over 100 countries around the world strategies for ensuring long-term persistence (rather (Langhammer et al. 2007: Appendix I). than simple short-term representation) of biodiversity Since the number of sites identified in such initia- (Pressey et al. 2004). However, assessing vulnerability tives is large, it has also proven possible to prioritize has proved problematic and various surrogates have among them by applying thresholds based on combi- been used to measure it. Wilson et al. (2005) catego- nations of vulnerability and irreplaceability. Ricketts et rized these into 4 groups based on types of data used: al. (2005) identified sites known to hold the entire pop- tenure and land use; environmental or spatial vari- ulation of at least one Critically Endangered or Endan- ables; threatened species data; and expert opinion. gered species — sites where species extinctions will Here we focus on the third of these. Threatened spe- occur unless immediate conservation action is taken. cies data (threat ranking and associated spatial attrib- The nested nature of these high priority sites as a sub- utes) have many advantages, among them the ability set of other site-scale conservation targets (specifically to integrate information across threatening processes, KBAs, and their avian subset) is illustrated in Fig. 5, some of which are otherwise difficult to map regionally relative to the coarse-scale analysis of Rodrigues et al. or globally (e.g. invasive species, hunting), or are diffi- (2004a), who used extent of occurrence data, demon- cult to measure (e.g. habitat degradation and loss in strating how the different resolutions of spatial data arid regions) (Wilson et al. 2005). Furthermore, IUCN can be used to highlight priorities at different scales (see Reid 1998). 2Sites are defined as discrete areas that: (1) are different in character or habitat or ornithological importance from their surrounding areas; (2) exist as actual or potential protected CONSIDERATIONS AND CHALLENGES areas or as areas which can be managed in some way for nature conservation; and (3) are, alone, or with other sites, self-sufficient areas which provide all the requirements of Although increasingly recognized and employed as the species, when present, for which they are important a tool for conservation planning, there are several con- (Fishpool & Evans 2001) siderations that need to be borne in mind when using 118 Endang Species Res: 6:113–125, 2008

Fig. 3. Global distribution of (a) irreplaceability, (b) threat, and (c) priority for the expansion of the global protected-area network for the conservation of species of mammals, amphibians, turtles and threatened birds. Irreplaceability value ranges from 0% (a site that is not needed to achieve target goals) to 100% (a site for which there are no other replacements); threat values correspond to those calculated based on the extinction risk indicator of Butchart et al. (2004). The highest priority sites, shown in (c), are those that fall simulataneously into the higher classes of irreplaceability value (≥0.9) and threat value (the top 5% in val- ues of the extinction risk indicator). (Figure reproduced, with permission, from Rodrigues et al. 2004b; ©American Institute of Biological Sciences)

Fig. 4. The 7504 confirmed Important Bird Areas (IBAs) of global significance identified as of February 2008, based on the presence of significant populations of threatened species, restricted-range species, biome-restricted species, and congregatory species (data courtesy of BirdLife International). IBA identification is underway for Antarctica, Australia, New Zealand, Melanesia, Brazil and the southern cone, Mexico, and North America Hoffmann et al.: Conservation planning and the IUCN Red List 119

servation (e.g. Possingham et al. 2002). Indeed, the most common misuse of the IUCN Red List involves taking threat rankings at face value to define priorities. The IUCN explicitly notes, ‘…The category of threat is not necessarily sufficient to determine priorities for conservation action. The category of threat simply pro- vides an assessment of the extinction risk under cur- rent circumstances’ (IUCN 2001). This does not reduce the value of the IUCN Red List, when correctly used, for informing spatial and tempo- ral options in conservation planning, but it does mean that other relevant considerations, such as opportuni- ties and costs (Wilson et al. 2006) should be incorpo- rated. For example, species-based irreplaceability data and species-based threat data can yield a set of priority sites, such as a set of IBAs, for a given region. How- ever, additional information must be incorporated through another type of vulnerability: site-based threat, i.e. a measure of threatening processes acting on each particular site. While species-based threat indicates whether the species occurring at a site has a high probability of global extinction, site-based threat informs the probability of that species’ local extirpation through site destruction/degradation. Integrating this additional information greatly improves the prioritiza- tion results, thus maximizing the practical usefulness of the IUCN Red List data. Unfortunately, no mecha- Fig. 5. Conservation priorities at the site scale in Madagascar, nism currently exists for compiling information on site- as determined using IUCN Red List data: Key Biodiversity Ar- level threat in a systematic and standardized way, eas (KBA; n = 117) identified from the distributions of threat- although BirdLife’s IBA monitoring framework pro- ened species covering 8 taxonomic groups (mammals, birds, amphibians, freshwater fishes, reptiles, arthropods, gastro- vides a simple and repeatable system for assessing and pods and plants) (preliminary data from Z. L. Rakotobe et al. monitoring degree of threat to sites and is now being unpubl. data); Important Bird Areas (IBA; n = 78), the avian implemented globally. subset of KBAs (modified from Fishpool & Evans 2001); and Alliance for Zero Extinction (AZE) sites (n = 16), the highest priority sites for biodiversity conservation, containing the en- tire population of at least one Critically Endangered or Species concepts Endangered species (modified from Ricketts et al. 2005 using data from AZE; www.zeroextinction.org, v2.1). Inset: urgent The influence of differing species concepts on the priorities (pink grid squares) for expanding the network of 1 IUCN Red List has some relevance to conservation protected areas in Madagascar (at a ⁄4-degree grid cell) ranked according to an Extinction Risk Index (data for mam- planning. The Biological Species Concept (Mayr 1963) mals, birds, amphibians and turtles; modified from Rodrigues has been the primary one used to date both in the et al. 2004a) IUCN Red List and in conservation planning. However, the increasing use of a Phylogenetic Species Concept (PSC; Cracraft 1983, Nixon & Wheeler 1990) will lead the IUCN Red List for this purpose. We review some of to a much larger number of species being recognized these here, and highlight challenges that must be met (termed ‘taxonomic inflation’: Isaac et al. 2004, Mace in order to ensure that the IUCN Red List improves as 2004). Agapow et al. (2004) have estimated that adop- a functional tool for conservation planners. tion of the Phylogenetic Species Concept would result in a 48% increase in species numbers and an uplisting of 11% of species from Vulnerable to Endangered. Threatened species lists and conservation planning This mainly occurs when ‘splitting’ biological species and subspecies into phylogenetic species, since this As with any threatened species list, the IUCN Red has direct influence on overall population size and List alone is not sufficient to determine the priority geographic range size, key factors inherent in the allocation of resources for area-based biodiversity con- IUCN Red List criteria (Collar 1996b). Not only would 120 Endang Species Res: 6:113–125, 2008

this lead to dilution of existing priorities with a flood of Improving the rigor of IUCN Red List assessments phylogenetic species (Collar 1997), but its patchy adoption to date has already resulted in inequalities in Independent evaluations of several threatened spe- world species lists (Collar 2003), and concomitant tax- cies categorization systems have shown the IUCN Red onomic biases in the number of threatened species. List to be the most suitable for assessing species extinc- Whereas some studies indicate that use of different tion risk (e.g. De Grammont & Cuaron 2006). However, species concepts will produce different sets of priority despite development of objective criteria (and a Users conservation areas (e.g. Peterson & Navarro-Sigüenza Working Group and Standards and Petitions Working 1999), others suggest that general biodiversity pat- Group within IUCN to promote consistency), consis- terns will not differ too greatly, at least at coarse tency and subjectivity in the application of these within scales (e.g. Dillon & Fjeldså 2005). Even at the finer and across taxa remains an issue (Keith et al. 2004). scale, changing taxonomy may yield little in the way The IUCN Red List criteria are designed to handle of new conservation insights in terms of priorities uncertainty (Akçakaya et al. 2000), but when there is (Collar 2007). An alternative approach is to directly inadequate information to make an assessment of incorporate phylogeny into priority setting (Crozier extinction risk, the category Data Deficient must be 1997, Isaac et al. 2007), although simulations suggest used. Overly precautionary listing of Data Deficient this may be unnecessary (Rodrigues et al. 2005). species as threatened sometimes stems from concerns BirdLife International are currently developing crite- that species listed as Data Deficient are seldom benefi- ria for recognizing species limits in order to apply a ciaries of conservation investment (e.g. see Garnett et global standard and establish a consistent approach to al. 2003). Such an approach to listing can lead to a con- bird taxonomy. This seems all the more necessary in fusion of conservation priorities with research priori- light of, for example, Garnett & Christidis (2007), who ties, and movement of valuable conservation resources warn that the adoption of a PSC in the IUCN Red List away from species that need them most. Furthermore, would incur substantial transaction and opportunity classification in the Data Deficient category does not costs with only marginal benefit for biodiversity con- imply lack of threat; The Standards and Petitions servation. Working Group (2006) explicitly notes ‘it may be appropriate …to give them the same degree of atten- tion as threatened taxa until their status can be Omission and commision errors assessed.’ Accordingly, a few conservation funds, such as the Conservation Leadership Programme Systematic conservation planning is sensitive to (http://conservation.bp.com/), explicitly call for pro- errors in the underlying species data. The errors fac- posals for research on Data Deficient species. ing species distribution data can be divided into 2 Conversely, listing species genuinely threatened classes: errors of commission (when a species is mis- with extinction as Data Deficient, either because asses- takenly thought to be present and adequately pro- sors demand substantial evidence that a species is tected at site where it does not occur) and errors of threatened before making such a classification, or to omission (when a species is mistakenly thought to be side-step well intentioned but misguided government absent from a site where it could be protected). policies that restrict field research on threatened spe- Where the goal is to prevent extinctions, omission cies, could result in such species not receiving conser- errors are much less dangerous, although they remain vation attention before it is too late (Pimenta et al. problematic because they reduce the number of spa- 2005, Stuart et al. 2005). Improved training in the use tial options available for conservation plans and tend of the IUCN Red List criteria, particularly at a regional to result in reserve systems that are inadequate across level, and assessor awareness of issues relating to cri- species ranges. Commission errors, by contrast, could teria application can help ensure consistency and min- lead to species extinction, because conservationists imize discrepancies between the global IUCN Red List could assume a species is conserved where it does not and national Red Lists. actually occur (Rondinini et al. 2006, Langhammer et al. 2007). EOO ranges (such as those generated as supporting documentation to the IUCN Red List Capacity assessments) may generate large commission errors if used in a manner that assumes homogenous species Perhaps the greatest challenge to the IUCN Red List distributions; point locality data (such as those which is capacity. For example, assessments for all of inform identification of IBAs and KBAs) can minimize Ecuador’s endemic plants, some 4000 species, were commission errors, but may contain large omission completed by Valencia et al. (2000); to date, just 2159 errors (Rondinini et al. 2006). species have been incorporated into the IUCN Red Hoffmann et al.: Conservation planning and the IUCN Red List 121

List. These delays are due to the time taken for exten- first-ever global assessment of, among other groups, all sive peer review of all assessments, which is exacer- the world’s sharks and reef-building corals soon to be bated by the need for translation. Clearly, expediting completed. Such assessments are now gaining traction assessment and subsequent integration of nationally in international mandates, for example, as Target 2 of and regionally endemic species into the global IUCN the ‘2010 Global Strategy for Plant Conservation’ Red List is a top priority. While the above example (www. biodiv.org/) of the Convention on Biological highlights the need for increased centralized capacity, Diversity, which calls for ‘a preliminary assessment of it is also necessary to encourage and facilitate national the conservation status of all known plant species’ by or regional IUCN Red Listing efforts that involve 2010. appropriate application of the regional guidelines and Existing conservation planning efforts using IUCN that include full supporting documentation. Partly to Red List data will often be setting priorities based on support this, IUCN’s Species Survival Commission our knowledge of the best-known taxa, particularly (SSC) runs regional IUCN Red List assessor-training vertebrates; other taxa also in need of conservation workshops (Hilton-Taylor et al. 2000). In the interim, attention may, unnervingly, be falling through the data originating from regional Red Listing initiatives cracks. Several analyses have revealed, for example, can usefully inform regional-level conservation plan- that freshwater taxa — both fish and invertebrates — ning exercises, provided these data are used in tandem are among the most threatened in the world (Mace et with existing global-level species data (see ‘Global al. 2005). However, they are also poorly studied and standardization’). the coverage within the IUCN Red List is limited, although initiatives are underway to expedite the assessment of freshwater species globally (e.g. Darwall Coverage et al. 2005, Kottelat & Freyhof 2007). This suggests that due to a lack of knowledge of the status of many taxo- Whereas some taxa have been comprehensively nomic groups, conservation planners will need to rely, assessed (all birds have been assessed 4 times since for now, on what we do know to serve as surrogates for 1988; BirdLife International 2004a3), taxonomic and the purpose of setting conservation priorities. Encour- geographic biases exist. Around 41 000 (2%) of cur- agingly, several recent studies (Brooks et al. 2001, Pain rently described species worldwide have been evalu- et al. 2005, Tushabe et al. 2006) have shown that, at ated using the IUCN Red List categories and criteria. least among IBAs, these sites successfully represented Only 4% of plants have been evaluated globally wider biodiversity, with Uganda’s IBA network, for against the criteria, and a quarter of these are from example, capturing at least 70% of the country’s but- Ecuador. Only 2 plant groups — cycads (Donaldson terfly and woody plant species, 86% of its dragonflies 2003) and conifers (Farjon & Page 1999) — have been and 97% of its birds. Such results suggest that, while comprehensively (i.e. all species) assessed to date. by no means complete, a set of sites identified based on Clearly, improved coverage of the IUCN Red List has only a single taxon (in this case, IBAs) represents a direct relevance for conservation planning purposes. central core of key sites upon which to build. More The most effective leaps forward in expediting list- generally, a recent synthesis of studies of surrogacy in ings into the official IUCN Red List, and reducing geo- biodiversity conservation suggests that, while never graphic and taxonomic biases, will be made through perfect, cross-taxonomic surrogacy tends to be posi- the ‘global assessments’. These initiatives coordinate tive, and that conservation planning based on data for status evaluations of all species in major taxonomic well-known taxonomic groups can proceed, albeit cau- groups, incorporating inputs by IUCN/SSC Specialist tiously, under the assumption that it captures species Groups where these exist, and following the approach in less well-known taxa within the same realm of BirdLife International. Global assessments maxi- (Rodrigues & Brooks 2007). mize use of available resources and expert opinion to produce standardized, peer-reviewed, detailed accounts of the status of large numbers of species. The Knowledge Global Amphibian Assessment was completed in 2004 (Stuart et al. 2004); a major reassessment of the world’s Even amongst the best-known species, gaps in mammals is due to be launched late 2008, and a Global knowledge remain. There is insufficient information Marine Species Assessment is underway, with the on many species in globally assessed groups to make an adequate IUCN Red List assessment (e.g. 23% of amphibians; ~1% of birds) and so they are listed as 3A fifth, complete assessment of all birds is due on 19 May Data Deficient. This can help highlight regions requir- 2008 (see www.birdlife.org) ing much additional survey work, such as the poorly 122 Endang Species Res: 6:113–125, 2008

studied New Guinea region, where 23% of Data Defi- where the species are still abundant have a special cient birds are found (Baillie et al. 2004). Change in responsibility to invest in their conservation and knowledge may also result in species moving from one ensure its security. For example, the dugong Dugong category of threat to another; for example, 139 birds dugon is listed as Vulnerable on the IUCN Red List, but underwent a change in IUCN Red List category is not listed on the Australian National Red List, a between 2000 and 2004 due to improved information country that harbors globally significant populations of on their distribution, population, trends and threats the species. Conservation planning and action takes (Butchart et al. 2004). Such changes do not invalidate place at a sub-global scale, and so it is key that the the use of IUCN Red List data in conservation plan- global context is taken into account to ensure that ning, but conservation planners need to be iterative in these actions are complementary to global conserva- setting priorities based on the best knowledge avail- tion efforts. able at the time. Consequently, conservation planners should be aware that, relative to regions where knowl- edge gaps are minimal, their understanding of the con- CONCLUSIONS servation importance of poorly known regions is likely to change considerably. The IUCN Red List is now widely applied in conser- vation planning at various scales, particularly in the identification of site-based conservation targets. Such Global standardization targets are slowly gaining formidable traction in national legislation: for example, the President of Sub-global Red Lists now exist for many countries the Philippines, Gloria Macapagal-Arroyo, signed an and regions. On the one hand, these are important for Executive Order in November 2006 mandating the national policy (Miller et al. 2006), and sometimes management and protection of KBAs as critical habi- incorporate data of higher quality than those utilized tats under the Philippine Wildlife Act. Although con- globally (Rodriguez et al. 2000). On the other hand, servation priorities generally should not be determined these lists may be hampered by strongly evidentiary or using threatened species lists alone, the practical value precautionary approaches to IUCN Red Listing (Stuart of the IUCN Red List in informing conservation plan- et al. 2005), inconsistent use of IUCN Red List criteria, ning at multiple scales has been demonstrated and is and/or lack of sufficient transparent documentation to therefore likely to increase. In this regard, a comple- ensure assessments can feed through to the global mentary future direction will be the development of a IUCN Red List (Hilton-Taylor et al. 2000). In order to quantitative methodology and criteria for measuring support regional listing efforts, IUCN has produced the threats at the site level (Langhammer et al. 2007). extensive guidelines for their application at the Some tough challenges remain to ensure that the regional level (Gärdenfors et al. 2001, IUCN 2003) — IUCN Red List continues to develop as a functional tool although there have been several calls for these to be in the conservation planner’s toolbox, but these should refined (e.g. Eaton et al. 2005) — and appointed a not detract from its value in helping to inform both National Red List Working Group to encourage best temporal and spatial options for conservation plan- practice in national Red Listing efforts. ning, thereby assisting in the selection of priority areas Individual countries, of course, have a responsibility for biodiversity conservation on the ground. to protect their national biodiversity assets. However, for the purposes of global conservation priority setting Acknowledgements. We thank Leon Bennun, Luigi Boitani, and planning, species listed on regional Red Lists but Stuart Butchart, Nigel Collar, Holly Dublin, Graham Edgar, which are not globally threatened or country endemics John Lamoreux, Craig Hilton-Taylor, David Knox, Georgina do not have the same currency as those that are glob- Mace, Michael Samways, Ali Stattersfield, Simon Stuart, and 4 anonymous reviewers for their valuable comments and help ally threatened on the IUCN Red List (Hilton-Taylor et with this manuscript. al. 2000). There is an inherent bias in regional Red Lists towards locally rare, but globally widespread, species (particularly those at the edges of their ranges). LITERATURE CITED For example, the herald petrel Pterodroma heraldica, Agapow PM, Bininda-Emonds ORP, Crandall KA, Gittleman listed as Least Concern on the global IUCN Red List is JL, Mace GM, Marshall JC, Purvis A (2004) The impact of considered Critically Endangered on the Australian species concept on biodiversity. Q Rev Biol 79:161–179 National Red List, because it is threatened in the small Akçakaya HR, Ferson S, Burgman MA, Keith DA, Mace GM, Todd CR (2000) Making consistent IUCN classifications fraction of its total range that enters Australian territo- under uncertainty. Conserv Biol 14:1001–1013 rial waters. Likewise, species may be globally threat- Anderson S (2002) Identifying important plant areas. Plantlife ened, but locally common, in which case countries International, London Hoffmann et al.: Conservation planning and the IUCN Red List 123

Baillie JEM, Bennun LA, Brooks TM, Butchart SHM and oth- Danielsen F, Treadaway CG (2004) Priority conservation ers (2004) 2004 IUCN Red List of Threatened Species. A areas for butterflies (Lepidoptera: Rhopalocera) in the Global Species Assessment. IUCN, Gland and Cambridge Philippine islands. Anim Conserv 7:79–92 BirdLife International (2004a) State of the World’s Birds 2004: Darwall WRT, Vié JC (2005) Identifying important sites for indicators for our changing world. BirdLife International, conservation of freshwater biodiversity: extending the Cambridge species-based approach. Fish Manag Ecol 12:287–293 BirdLife International (2004b) Tracking ocean wanderers: the Darwall W, Smith K, Lowe T, Vié JC (2005) The status and dis- global distribution of albatrosses and petrels. Results from tribution of freshwater biodiversity in Eastern Africa. the Global Procellariiform Tracking Workshop, 1–5 Sep- IUCN/SSC Freshwater Biodiversity Assessment Pro- tember, 2003, Gordon’s Bay, South Africa. BirdLife Inter- gramme. IUCN, Gland and Cambridge national, Cambridge De Grammont PC, Cuaron AD (2006) An evaluation of threat- Boyd C, Brooks TM, Butchart SHM, Edgar GJ and others (in ened species categorization systems used on the American press) Scale and the conservation of threatened species. continent. Conserv Biol 20:14–27 Conserv Lett Dillon S, Fjeldså J (2005) The implications of different species Brooks T, Balmford A, Burgess N, Hansen LA and others concepts for describing biodiversity patterns and assess- (2001) Conservation priorities for birds and biodiversity: ing conservation needs for African birds. Ecography Do East African Important Bird Areas represent species 28:682–692 diversity in other terrestrial vertebrate groups? Ostrich Donaldson JS (ed) (2003) Cycads. Status survey and conser- 15:3–12 vation action plan. IUCN/SSC Cycad Specialist Group. Brooks TM, Bakarr MI, Boucher T, da Fonseca GAB and oth- IUCN, Gland and Cambridge ers (2004) Coverage provided by the global protected- Eaton MA, Gregory RD, Noble DG, Robinson JA and others area system: Is it enough? Bioscience 54:1081–1091 (2005) Regional IUCN Red Listing: the process as applied to Brooks TM, Mittermeier RA, da Fonseca GAB, Gerlach J and birds in the United Kingdom. Conserv Biol 19:1557–1570 others (2006) Global biodiversity conservation priorities. Eken G, Bennun L, Brooks T, Darwall W and others (2004) Science 313:58–61 Key Biodiversity Areas as site conservation targets. Bio- Bruner AG, Gullison RE, Rice RE, Fonseca GAB (2001) Effec- science 54:1110–1118 tiveness of parks in protecting tropical biodiversity. Farjon A, Page CN (compilers) (1999) Conifers. Status survey Science 291:125–128 and conservation action plan. IUCN/SSC Conifer Special- Butchart SHM, Stattersfield AJ, Bennun LA, Shutes SM and ist Group. IUCN, Gland and Cambridge others (2004) Measuring global trends in the status of bio- Fishpool LDC, Evans MI (2001) Important Bird Areas in Africa diversity: Red List Indices for birds. PLoS Biol and associated islands: Priority sites for conservation. 2(12):2294–2304 Pisces Publications and BirdLife International, Newbury Collar NJ (1993–4) Red data books, action plans, and the and Cambridge need for site-specific synthesis. Species 21 and 22: Fitter R, Fitter M (1987) The road to extinction: problems of 132–133 categorizing the status of taxa threatened with extinction. Collar NJ (1996a) The reasons for Red Data Books. Oryx IUCN, Gland and Cambridge 30:121–130 Gärdenfors U, Hilton-Taylor C, Mace GM, Rodriguez JP Collar NJ (1996b) Species concepts and conservation: a (2001) The application of IUCN Red List criteria at response to Hazevoet. Bird Conserv Int 6:197–200 regional levels. Conserv Biol 15:1206–1212 Collar NJ (1997) Taxonomy and conservation: chicken and Garnett SC, Christidis L (2007) Implications of changing spe- egg. Bull Br Ornithol Club 117:122–136 cies definitions for conservation purposes. Bird Conserv Collar NJ (2003) How many bird species are there in Asia? Int 17:187–195 Oriental Bird Club Bull 38:20–30 Garnett S, Crowley G, Balmford A (2003) The costs and effec- Collar NJ (2007) Philippine bird taxonomy and conservation: tiveness of funding the conservation of Australian threat- a commentary on Peterson (2006). Bird Conserv Int ened birds. Bioscience 53:658–665 17:103–113 Gascon C, Williamson GB, da Fonseca GAB (2000) Receding Collar NJ, Stuart SN (1985) Threatened birds of Africa and forest edges and vanishing reserves. Science 288: related islands: the ICBP/IUCN Red Data Book. Third edi- 1356–1358 tion, part 1. International Council for Bird Preservation, Hilton-Taylor C, Mace GM, Capper DR, Collar NJ and others and International Union for Conservation of Nature and (2000) Assessment mismatches must be sorted out: they Natural Resources, Cambridge leave species at risk. Nature 404:541 Collar NJ, Stuart SN (1988) Key forests for threatened birds in Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its Africa. International Council for Bird Preservation and influence on macroecology and conservation. Trends Ecol IUCN, Evol 19:464–469 Cowling RM, Pressey RL, Rouget M, Lombard AT (2003) A Isaac NJB, Turvey ST, Collen B, Waterman C, Baillie JEM conservation plan for a global biodiversity hotspot — the (2007) Mammals on the EDGE: conservation priorities Cape Floristic Region, South Africa. Biol Conserv based on threat and phylogeny. PLOS One 2(3):e296 112:191–216 IUCN (1994) IUCN Red List Categories. IUCN Species Sur- Cracraft J (1983) Species concepts and speciation analysis. vival Commission. IUCN, Gland Curr Ornithol 1:159–187 IUCN (2001) IUCN Red List Categories and Criteria: version Crozier RH (1997) Preserving the information content of spe- 3.1. IUCN, Gland and Cambridge cies: genetic diversity, phylogeny, and conservation IUCN (2003) Guidelines for Application of IUCN Red List worth. Annu Rev Ecol Syst 28:243–268 Criteria at Regional Levels: Version 3.0. IUCN Species da Fonseca GAB, Sechrest W, Oglethorpe J (2005) Managing Survival Commission. IUCN, Gland and Cambridge the matrix. In: Lovejoy TE, Hannah L (eds) Climate Keith DA, McCarthy MA, Regan H, Regan T and others change and biodiversity. Yale University Press, New (2004) Protocols for listing threatened species can forecast Haven, CT extinction. Ecol Lett 7:1101–1108 124 Endang Species Res: 6:113–125, 2008

Kirkpatrick JB (1983) An iterative method for establishing pri- Possingham HP, Andelman SJ, Burgman MA, Medellin RA, orities for the selection of nature reserves — an example Master LL, Keith DA (2002) Limits to the use of threatened from Tasmania. Biol Conserv 25:127–134 species lists. Trends Ecol Evol 17:503–507 Komar O (2002) Priority conservation areas for birds in El Pounds JA, Bustamante MR, Coloma LA, Consuegra JA and Salvador. Anim Conserv 5:173–183 others (2006) Widespread amphibian extinctions from epi- Kottelat M, Freyhof J (2007) Handbook of European freshwa- demic disease driven by global warming. Nature 439: ter fishes. Published by the authors, ISBN: 9782839902984 161–167 Lamoreux J, Akçakaya R, Bennun L, Collar NJ and others Pressey RL, Taffs KH (2001) Scheduling conservation action (2003) Value of the IUCN Red List. Trends Ecol Evol in production landscapes: priority areas in western New 18:214–215 South Wales defined by irreplaceability and vulnerability Langhammer PF, Bakarr MI, Bennun LA, Brooks TM and oth- to vegetation loss. Biol Conserv 100:355–376 ers (2007) Identification and gap analysis of Key Biodiver- Pressey RL, Humphries CJ, Margules CR, Vane-Wright RI, sity Areas: targets for comprehensive protected area sys- Williams PH (1993) Beyond opportunism — key principles tems. IUCN, Gland for systematic reserve selection. Trends Ecol Evol 8: Mace GM (1995) Classification of threatened species and its 124–128 role in conservation planning. In: Lawton JH, May RM Pressey RL, Johnson IR, Wilson PD (1994) Shades of irreplace- (eds) Extinction rates. Oxford University Press, New ability — towards a measure of the contribution of sites to York a reservation goal. Biodivers Conserv 3:242–262 Mace GM (2004) The role of taxonomy in species conserva- Pressey RL, Cowling RM, Rouget M (2003) Formulating con- tion. Phil Trans R Soc Lond Ser B 359:711–719 servation targets for biodiversity pattern and process in Mace GM, Lande R (1991) Assessing extinction threats — the Cape Floristic Region, South Africa. Biol Conserv toward a reevaluation of IUCN threatened species cate- 112:99–127 gories. Conserv Biol 5:148–157 Pressey RL, Watts ME, Barrett TW (2004) Is maximizing pro- Mace GM, Baillie J, Masundire H, Ricketts TH and others tection the same as minimizing loss? Efficiency and reten- (2005) Biodiversity. In: Hassan R, Scholes R, Ash N (eds) tion as alternative measures of the effectiveness of pro- Ecosystems and human well-being. Vol 1. Current states posed reserves. Ecol Lett 7:1035–1046 and trends. Findings of the Condition and Trends Working Reid WV (1998) Biodiversity hotspots. Trends Ecol Evol Group. Millenium Exosystem Assessment series, Island 13:275–280 Press, Washington, DC Ricketts TH, Dinerstein E, Boucher T, Brooks TM and others Margules CR, Pressey RL (2000) Systematic conservation (2005) Pinpointing and preventing imminent extinctions. planning. Nature 405:243–253 Proc Natl Acad Sci USA 102:18497–18501 Master LL (1991) Assessing threats and setting priorities for Rodrigues ASL, Brooks TM (2007) Shortcuts for biodiversity conservation. Conserv Biol 5:559–563 conservation planning: the effectiveness of surrogates. Mayr E (1963) Animal species and evolution. Harvard Univer- Annu Rev Ecol Evol Syst 38:713–737 sity Press, Cambridge, MA Rodrigues ASL, Akçakaya HR, Andelman SJ, Bakarr MI and Miller RM, Rodriguez JP, Aniskowicz-Fowler T, Bamba- others (2004a) Global gap analysis: priorities for expand- radeniya C and others (2006) Extinction risk and conserva- ing the global protected area network. Bioscience 54: tion priorities. Science 313(5786):414 1092–1100 Mrosovsky N (1997) IUCN’s credibility critically endangered. Rodrigues ASL, Andelman SJ, Bakarr MI, Boitani L and Nature 389:436 others (2004b) Effectiveness of the global protected area Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, network in representing species diversity. Nature 428: Kent J (2000) Biodiversity hotspots for conservation priori- 640–643 ties. Nature 403:853–858 Rodrigues ASL, Brooks TM, Gaston KJ (2005) Integrating Nixon KC, Wheeler QD (1990) An amplification of the phylo- phylogenetic diversity in the selection of priority areas for genetic species concept. Cladistics 6:211–223 conservation: Does it make a difference? In: Purvis A, Git- Oliveira PJC, Asner GP, Knapp DE, Almeyda A and others tleman JL, Brooks TM (eds) Phylogeny and conservation. (2007) Land-use allocation protects the Peruvian Amazon. Cambridge University Press, Cambridge Science 317:1233–1236 Rodrigues ASL, Pilgrim JD, Lamoreux JL, Hoffmann M, Olson DM, Dinerstein E (1998) The Global 200: a representa- Brooks TM (2006) The value of the Red List for conserva- tion approach to conserving the earth’s most biologically tion. Trends Ecol Evol 21:71–76 valuable ecoregions. Conserv Biol 12:502–515 Rodriguez JP, Ashenfelter G, Rojas-Suarez F, Garcia Fernan- Orme CDL, Davies RG, Burgess M, Eigenbrod F and others dez JJ, Suarez L, Dobson AP (2000) Local data are vital to (2005) Global hotspots of species richness are not congru- worldwide conservation. Nature 403:241 ent with endemism or threat. Nature 436:1016–1019 Rondinini C, Stuart S, Boitani L (2005) Habitat suitability Osieck ER, Mörzer Bruyns MF (1981) Important Bird Areas in models and the shortfall in conservation planning for the European Community. International Council for Bird African vertebrates. Conserv Biol 19:1488–1497 Preservation, Cambridge Rondinini C, Wilson KA, Boitani L, Grantham H, Possingham Pain DJ, Fishpool L, Byaruhanga A, Arinaitwe J, Blamford A HP (2006) Tradeoffs of different types of species occur- (2005) Biodiversity representation in Uganda’s forest IBAs. rence data for use in systematic conservation planning. Biol Conserv 125:133–138 Ecol Lett 9:1136–1145 Peterson AT, Navarro-Sigüenza AG (1999) Alternate species Standards and Petitions Working Group (2006) Guidelines for concepts as bases for determining priority conservation using the IUCN Red List Categories and Criteria. Version areas. Conserv Biol 13:427–431 6.2. Prepared by the Standards and Petitions Working Pimenta BVS, Haddad CFB, Nascimento LB, Cruz CAG, Pom- Group of the IUCN SSC Biodiversity Assessments Sub- bal JBJ (2005) Comment on ‘Status and Trends of Amphib- Committee in December 2006 (available at http:// ian Declines and Extinctions Worldwide’. Science intranet.iucn.org/webfiles/doc/SSC/RedList/RedList 309:1999b Guidelines.pdf) Hoffmann et al.: Conservation planning and the IUCN Red List 125

Stattersfield AJ, Crosby MJ, Long AJ, Wege DC (1998) (2006) A nationwide assessment of the biodiversity value Endemic Bird Areas of the World: priorities for biodiversity of Uganda’s Important Bird Areas network. Conserv Biol conservation. BirdLife International, Cambridge 20:85–99 Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Valencia R, Pitman N, León-Yánez S, Jorgensen PM (eds) Fischman DL, Waller RW (2004) Status and trends of (2000) Libro Rojo de las plantas endémicas del Ecuador. amphibian declines and extinctions worldwide. Science Herbario QCA, Pontificia Universidad Católica del 306:1783–1786 Ecuador, Quito Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Walsh PD, Abernethy KA, Bermejo M, Beyers R and others Fischman DL, Waller RW (2005) Response to Comment on (2003) Catastrophic ape decline in western equatorial ‘Status and Trends of Amphibian Declines and Extinctions Africa. Nature 422:611–614 Worldwide’. Science 309:1999c Wilson K, Pressey RL, Newton A, Burgman M, Possingham H, Szaro RC, Johnston DW (eds) (1996) Biodiversity in managed Weston C (2005) Measuring and incorporating vulnerabil- landscapes: theory and practice. Oxford University Press, ity in conservation planning. Environ Manag 35:527–543 New York Wilson KA, McBride MF, Bode M, Possingham HP (2006) Pri- Tushabe H, Kalema J, Byaruhanga A, Asasira J and others oritizing global conservation efforts. Nature 440:337–340

Editorial responsibility: David Roberts, Submitted: November 22, 2007; Accepted: February 18, 2008 Kew, UK Proofs received from author(s): April 14, 2008